Catastrophic depletion of reef-associated sea …aspidolist.1006021.n3.nabble.com/attachment/448/0/HOL Lane... · coincident with the introduction of scuba and hookah diving to the

Catastrophic depletion of reef-associated sea cucumbers: resourcemanagement/reef resilience issues for an Indonesian marine park

and the wider Indo-Pacific

DAVID J. W. LANEa,b,* and DANIEL LIMBONGc,†

aDepartment of Biology, Universiti Brunei Darussalam, Brunei DarussalambHonorary Research Fellow, Raffles Museum of Biodiversity Research, Department of Biological Sciences, Faculty of Science, National

University of Singapore, SingaporecFaculty of Fisheries and Marine Science, Sam Ratulangi University, Kampus Unsrat, Bahu, Manado 95115, Sulawesi Utara, Indonesia

ABSTRACT

1. Commercial species of shallow-water, tropical, aspidochirotid sea cucumbers (bêche-de-mer) in the Indo-WestPacific, many of them, at maturity, large and conspicuous benthic members of coral reef or seagrass/sedimentenvironments, represent a high-value marine resource, traditionally fished for centuries, but which currently arebeing heavily overfished, largely through a growing demand from mainland China and regional markets in thesupply chain.

2. Population losses are exemplified by a study at Bunaken National Marine Park, North Sulawesi, Indonesia,where densities of commercial sea cucumber species are very low following earlier harvesting and where drop-outof species records has occurred over a 17-year study period.

3. Sea cucumber populations have not recovered from overexploitative depredations despite the designation ofthis area as a National Marine Park in 1991 and the commencement of protection measures.

4. This pattern of overexploitation, replicated across the tropical Indo-Pacific, has detrimental implications formany coastal communities traditionally or currently dependent on this high-value resource.

5. In addition there are potentially serious implications of overharvesting – reviewed here – for reef ecosystemresilience.Copyright # 2013 John Wiley & Sons, Ltd.

Received 29 July 2013; Revised 14 September 2013; Accepted 27 October 2013

KEY WORDS: Aspidochirotida; Bunaken; Echinodermata; Indo-Pacific; overfishing; reef resilience

*Correspondence to: D.J.W. Lane, Department of Biology, Universiti Brunei Darussalam, Jalan Tungku Link, BE1410, Brunei Darussalam. E-mail:[email protected]†Present address: Lembaga Penelitian dan Pengabdian Kepada Masyarakat Universitas Kristen Tentena, Jl. Torulemba No. 21, Tentena, Poso 94663,Sulawesi, Indonesia

Copyright # 2013 John Wiley & Sons, Ltd.

AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS

Aquatic Conserv: Mar. Freshw. Ecosyst. (2013)

Published online in Wiley Online Library(wileyonlinelibrary.com). DOI: 10.1002/aqc.2421

INTRODUCTION

Extraction of living resources from the sea, overperiods of decades to centuries, has resultedhistorically in serial catastrophic population declines,equating to ecological extinctions (Jackson et al.,2001; Pauly and Palomares, 2005) that areperceived to be a leading cause of ecologicalchange and collapse of many coastal ecosystemsworld-wide (Jackson et al., 2001). This patternof severe overfishing applies not only to finfish,marine mammals and invertebrate shellfish butto many other invertebrate resources too,including echinoderm species (Micael et al., 2009).Commercial species of aspidichirotid seacucumbers (Holothuroidea) are a case in point,with serial species overexploitation of thishigh-value product, known as bêche-de-mer, beinga characteristic pattern, particularly throughoutmuch of the tropical Indo-Pacific (Conand, 1998;Uthicke and Benzie, 2000; Uthicke et al., 2004;Conand and Muthiga, 2010; Purcell et al., 2010;Hamilton and Lokani, 2011). The multi-speciesglobal fishery for sea cucumbers has expandedrapidly in recent decades (Eriksson et al., 2012b)with the harvest peaking at about 130 000 metrictonnes (wet weight equivalent) of dried product,valued at about US$ 60 million, in 1995 (Jaquemetand Conand, 1999; Conand, 2001). Sea cucumbersare important to the economies and livelihoods ofmany coastal communities, particularly in thetropical Indo-Pacific, and are often the mosteconomically important fishery and non-finfishexport for many countries (Toral-Granda et al.,2008a). Sea cucumber fishers, estimated to numberaround 3 million (Purcell et al., 2011), representalmost half of the estimate for reef fishers globally(Teh et al., 2013). Overfishing of sea cucumbersthreatens the livelihood opportunities provided bythis high-value resource to coastal fishers (FAO,2013). As with other fishery resources, there isconcern that overfished bêche-de-mer stocks areslow to recover in population numbers or thatrecovery is lacking (Uthicke et al., 2004; Ahmedand Lawrence, 2007; Friedman et al., 2011; Priceet al., 2013). Furthermore, sustainable exploitationof sea cucumber stocks is, for many species,hindered by a number of biological and regulatory

factors: long life cycle (Uthicke et al., 2010) with,in many species, presumed slow development tomaturity; high visibility and accessibility ofshallow, sedentary species; low charismaticstanding (McClenachen et al., 2012); and lack ofany protection by CITES for almost all taxa(Purcell et al., 2010) despite good cases for listing(Bruckner et al., 2003). The recent IUCN listing ofseven commercial sea cucumber species asendangered with high risk of extinction (IUCN, 2013)is a welcome development but, in the tropicalIndo-Pacific at least, despite moratoria on exportsby some countries (Purcell et al., 2010; Friedmanet al., 2011), the fishery continues to be generallyunregulated or illegally overexploited and ischaracterized by an accelerating, large-scaleecosystem plunder (Toral-Granda, 2005 – Galapagos;Zabludovsky, 2013 – Mexico) that is evident formany other marine resources (Berkes et al., 2006).

Indonesia has the world’s largest fishery fortropical sea cucumber (Tuwo and Conand, 1992;Conand, 2001; Tuwo, 2004; Choo, 2008), yetmanagement of the fishery in the country has beenlimited or non-existent, species are merged in thetrade data (Choo, 2008), and field population datafor commercial species are sparse. Fishery data(Tuwo, 2004), although somewhat limited, do show adecline in size and catch per unit effort, indicatingthat bêche-de-mer species are generally beingoverexploited in the Archipelago. Hoeksema (2004)and Massin (1999) have noted the near disappearanceof commercial species over an approximate 10-yearperiod (mid-1980s to mid-1990s) around reefs of theSpermonde Archipelago, south-west Sulawesi,coincident with the introduction of scuba and hookahdiving to the fishery. This pattern of overexploitationand depletion of bêche-de-mer, characteristicthroughout the tropical Indo-Pacific (Toral-Grandaet al., 2008b; Hamilton and Lokani, 2011), seemed tobe evident in north Sulawesi too – at the BunakenNational Marine Park (BNMP) – and over a similartime period. This perception prompted a review ofthe first author’s detailed echinofaunal data recordsand photo records, obtained during a series ofechinoderm biodiversity scuba surveys at theBunaken Park over a 17-year period (1993–2010), aswell as a series of sea cucumber population densitysurveys in 2008. Initial observations in the early 1990s

D. J. W. LANE AND D. LIMBONG

Copyright # 2013 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. (2013)

indicated that while the species richness of seacucumbers appeared to be high, abundances werenot. High-value commercial bêche-de-mer species inparticular, all of them within the sediment-feedingorder Aspidochirotida, were uncommon or rare(Lane, 1999a), probably representing a legacy ofintensive harvesting and overexploitation in earlierdecades before establishment of the marinepark. Indeed, it has been reported that profitsfrom unrecorded and unregulated sea cucumberharvesting in the area were significant in supportingdevelopment of the local diving tourism industry inits early days (L. Herlambang pers. comm.).

BACKGROUND AND METHODOLOGY

The Bunaken National Marine Park, located at thenorthern tip of Sulawesi, near the geographic centreof the Coral Triangle (Briggs, 1974; Roberts et al.,2002; Hoeksema, 2007), includes five coralreef-fringed islands, part of the mainland coast ofthe north-western tip of Sulawesi, near Manadotown, and a separate section of coastal reefs atArakan-Wawontulap, south of Manado Bay(Figure 1). The park covers a marine domain of79 056 ha, including some 8010 ha of reef flat,slope and lagoonal habitat, the latter including atleast 1300 ha of seagrass beds (Mehta, 1999). Themarine park, formally established as Indonesia’sfirst National Marine Park by the IndonesianMinistry of Forestry in October 1991, is currentlyon the tentative list for World Heritage Site status(UNESCO, 2012). During the park’s initial years,management, monitoring and enforcement wereunder-resourced and there was evidence ofcontinued unsustainable fishing practices,particularly when, during the Asian economiccrisis of the late 1990s, cuts in conservationbudgets resulted in increased pressures on parkresources (Erdmann and Pet, 1999). However, thefall of the Soeharto regime following the Asianeconomic crisis of the late 1990s led ultimately togreater regional devolution in the Archipelago and,in turn, the development of a multi-stakeholderpark management structure (Bunaken NationalPark Management Advisory Board). Thismanagement board has, since March 2001,obtained revenue from park entrance fees, most of

which is directed towards conservation programmesand promotion of sustainable activities within thepark (Erdmann et al., 2004). The natural resourcesof the area and associated tourism support apopulation of some 30 000 residents (UNEP, 2005).

An aspidochirotid species list for BNMP wascompiled initially from echinofaunal checklistrecords and photorecords of the first author madeduring 14 scuba survey visits to both northern andsouthern sectors of the Bunaken Marine NationalPark, spanning a period of 17 years from June1993 to March 2010. Each visit lasted from 5 to 8days, with a combined total of 154 scuba dives.Each dive was of 1 h duration and 12 of themwere undertaken at night. Records of first andsubsequent sightings of sea cucumber taxa weremade photographically and/or tallied on acheck-list during the dives. Check-list records oftenconsisted of single occurrences during a dive. Thegeneral impression was that abundances of manysea cucumber species were low.

During a visit in December 2008 (13 dives),quantitative population studies were initiated inthe northern sector of the Park. These involved10m-wide belt transects on reef slope contoursbased on drift-dives of 1 h duration, andGPS-determined transect lengths ranging from300–790 m. An on-line utility (http://boulter.com/gps/distance/ ) is available to calculate the lineardistances between the GPS coordinates for the startand end points of transects. As sea cucumberencounters were relatively infrequent andunderwater visibility was high it was considered tobe more effective in terms of efficient use of divetime and areal coverage to set the belt width to10 m (with few or without replicates) rather thanthe more usual 2m-wide replicated transects. Thisprotocol, essentially a refinement of that adopted forearlier drift-dive surveys, avoided the problemsassociated with manta tows (e.g. missed individuals).The area covered and searched during each diveranged from 3000–7900 m2.

During the transect surveys all visible aspidochirotidsea cucumbers, i.e. diurnally active, epibenthic andsemi-cryptic individuals within a gauged 10m trackwidth were recorded on a species list, counted, andmeasured for length. The semi-cryptic forms includedindividuals either partially hidden in recesses, covered

CATASTROPHIC BÊCHE-DE-MER DEPLETION


http://boulter.com/gps/distance/

http://boulter.com/gps/distance/

by rock slabs or a layer of debris, or semi-buried insediment. Belt transect survey coverage included reefslopes at depths of 5–25 m around three of the largerislands in the northern BNMP sector, namelyBunaken, Manado Tua and Mantehage, plus

mainland reef slopes within the northern park sector.No attempt was made to quantify sea cucumberrecords or densities for reef flat species or fornocturnal species observed during night dives,although these records contributed to a species

Figure 1. Map of Bunaken National Marine Park, North Sulawesi, Indonesia. Locations of quantitative transect surveys for aspidochirotid seacucumbers are indicated by stars.



richness assessment. Identifications were based on insitu colour slide or digital photographs, the primaryand revisionary taxonomic literature and a recentguide book on commercial sea cucumbers (Purcellet al., 2012).

RESULTS

Species richness

Species records for aspidochirotid sea cucumbers inthe BNMP during the series of 14 surveys, from

Table 1. Bunaken Marine Park aspidochirotid counts by species for swim-line surveys, 1993-2010. The December 2008 column (shaded) representsdata acquired using a different protocol (belt-transects). Species value categories derived from Choo, 2008, Conand, 2008, Kinch et al., 2008b,Purcell et al., 2010, 2012. NA designates either ‘not applicable’ for species not known to occur in the fishery, or ‘not available’ for fished butunrecognized species. Boldened names represent species recently categorized (IUCN, 2013) as Endangered (E) or Vulnerable (V) to extinction



Tab

le2.

Aspidochirotid

seacucumbercoun

tsanddensities,B

unaken

MarinePa

rkbelt-transectsurveys,Decem

ber2008.C

ountsarebo

ldened

anddensities

(num

bersperhectare)arein

parentheses.

HV:h

ighvalue;MV:m

edium

value;LV:low

value;NA:n

otapplicable(species

unkn

ownor

unrecognized

inthefishery)

Survey

location

Bun

aken,

Fuk

uiS.W.

Bun

aken,

Alung

Ban

uaMan

teha

geN.W

.Man

teha

geS.

(Ban

gopt.)

Bun

aken

N.E.

Man

teha

geE.

Man

teha

geS.E.

Man

ado

Tua

,N.E.

Bun

aken,

Fuk

uito

Alung

aban

uaBun

aken

Fuk

uiMainlan

d,nr.T

iwoh

oMainlan

d,W.

ofTiwoh

o

Survey

Areaha

0.4

0.5

0.62

0.4

0.5

0.3

0.4

0.32

0.79

0.38

0.62

0.4

Market

value

Tax

on

HV

Holothuria

fuscogilva

1(3.33)

1(2.5)

2(5.26)

MV

Actinopyga

palauensis

2(4)

Bohadschia

argus

7(14)

1(1.61)

2(5)

1(2)

6(7.6)

1(2.63)

3(4.82)

1(2.5)

LV

Bohadschia

marmorata

1(3.33

Holothuria

coluber?

1(3.33)

Holothuria

fuscopunctata

2(5)

1(2)

1(1.27)

1(2.63)

1(1.61)

Pearsonothuria

graeffei

1(2.5)

2(4)

22(35.48)

5(10)

4(10)

2(6.19)

2(2.53)

5(13.16)

3(4.82)

6(15)

Thelenota

anax

3(6)

1(2.5)

1(3.1)

6(7.6)

3(4.82)

Thelenota

rubralineata

1(2.53)

NA

Holothuria

edulis(pink)

2(4)

2(4)

1(3.1)

1(1.61)



1993 to 2010, are given in Table 1. The fauna list(28 species) includes several records of rare orrecently described Indo-Pacific species, e.g.Actinopyga caerulea (Samyn et al., 2006), Stichopusocellatus (Massin et al., 2002) and Thelenotarubralineata (Massin and Lane, 1991). The inventoryalso includes two rarely encountered species,Holothuria whitmaei and Thelenota ananas (Table 1),categorized recently as endangered by theInternational Union for the Conservation of Nature(IUCN, 2013).

Abundances and population densities

Records for high-value aspidochirotids during the17-year series of swim-line surveys often consistedof low numbers or singletons (Table 1). Highercounts in June 2009 are attributed to an observereffect, there being two observer divers at that timecompared with a single observer on other swim-linesurveys. Belt-transect surveys in December 2008(Table 1 – highlighted column) resulted in lowencounter rates for high-value species and lowdensities for most species (Table 2). In thesequantitative surveys the most abundant seacucumber, Pearsonothuria graeffei, a low-valuespecies with a thin body wall, had a peak density of35 ind. ha-1. In contrast, except for themedium-value species Bohadschia argus at one site,the densities for medium- and high-value specieswere less than 10 ind. ha-1 (Table 2). In fact duringthe belt transect surveys only one high-value species,Holothuria fuscogilva, was found (Table 2) and

other high-value species, recorded in previousBNMP surveys, were not seen. Low frequency ofencounters is apparent in the high-value speciesrecords for surveys before 2008 (Table 1) anddrop-out of certain taxa is apparent. For example,one of the highest value species, Holothuriawhitmaei, has not been seen since March 2000 andthe medium-value Actinopyga echinites andStichopus herrmanni, both considered vulnerable toextinction (IUCN, 2013), have not been seen sincesingleton records in 1994 (Table 1).

Size composition of populations

Size–frequency plots (Figure 2), derived from theDecember 2008 transect survey data, aremeaningful only for those species that weresufficiently abundant (barely in some cases). Themost abundant species, Pearsonothuria graeffeiand Bohadschia argus show a normal distribution,peaking in abundance in the 30–40 cm size class.It should be noted, however, that the reliability oflength data for P. graeffei is influenced by the factthat undisturbed individuals are frequently foundin varied states of contraction or extension.Thelenota anax was generally found as large tovery large individuals and no individuals under30 cm in length were seen. Size–frequency plotsare given for two other commercial species,Holothuria fuscogilva and Holothuria fuscopunctata(Figure 2); the data are too few to show patternsof population size structure clearly, but againsmall individuals are very few or absent.

DISCUSSION

The series of visits to BNMP revealed a highaspidochirotid species richness (28), consistentwith the location at the geographic centre of thezone of maximum marine biodiversity, butabundances were low – an observation whichstimulated the quantitative aspects of this study. Incontrast, observations for nocturnally activespecies indicated much higher numbers anddensities. Night surveys were not quantitativebecause of logistic difficulties but large nocturnalspecies, notably Stichopus noctivagus and

Figure 2. Size–frequency plot for the five most abundant species in theDecember 2008 belt- transect surveys at Bunaken National Marine Park.



Holothuria turriscelsa, were commonly seen (> 10individuals per dive) on the reef slopes and wallsduring night dives at Bunaken Island. These twonocturnally emergent species are not currently onthe list of commercially targeted species but manyother burrowing forms are (Kinch et al., 2008a).Cryptic behaviour in nocturnal species – hidingwithin the reef matrix or sediment by day andemerging only after sunset – may afford them someprotection from harvesting (but see comments below).

Bêche-de-mer population densities measuredduring the series of surveys in December 2008 arevery low, except for the thin-walled, low-valuePearsonothuria graeffei at some sites (Table 2). Allother species, including high- and medium-valueones, occurred at densities of less than 10 ind. ha-1

(except for the medium-value Bohadschia argus atone transect site). Low densities and drop-out ofspecies records for these large, conspicuousinvertebrates at BNMP is indicative ofoverexploitative extraction of this resource.Similar low densities have been recorded forheavily fished localities in the western centralPacific (Kinch et al., 2008a). The most strikingfinding of the recent (December 2008) quantitativesurvey is the absence from the transect census ofseveral high-value species previously recorded inBNMP, notably Holothuria whitmaei, Holothuriascabra, Stichopus herrmanni and Thelenota ananas(Table 2). Thelenota ananas (the prickly redfish),formerly one of the more abundant and widelydistributed large stichopodid sea cucumbers in thetropical west Pacific (personal observation of firstauthor), is now considered endangered withextinction (IUCN, 2013). At Bunaken, and manyother locations, it is now rarely sighted, unlike itslower value congeners T. anax (Tables 1, 2) and,in some locations, T. rubralineata (Lane, 1999b,2008). The only high-value species recorded in theBNMP transect surveys, Holothuria fuscogilva,occurred at low population densities of 2.5–5.3ind. ha-1. Low count rates or total absence(combined survey area of 5.6 ha) indicate thatstocks of many high-value species are indeed verylow on reefs within the marine park.

Density values for large-bodied, commerciallytargeted sea cucumbers are typically much higheron protected or underexploited reefs in the tropical

Indo-Pacific. For example, Holothuria whitmaei(the black teatfish), Holothuria fuscogilva (thewhite teatfish) and Holothuria scabra (the sandfish) were reported to occur at peak densities of30, 50 and 500 ind. ha-1, respectively, on theunfished reefs of Eastern Torres Strait (Long andSkewes, 1997). For H. whitmaei, one of the mostvaluable species in the west Pacific, densities atprotected sites on the Great Barrier Reef (about 20ind. ha-1) were about four times the values forfished reefs (Uthicke and Benzie, 2000 – asH. nobilis). Population densities of H. whitmaeiabove 12.5 ind. ha-1 are characteristic of protectedor unfished reefs and are considered by Kinchet al. (2008a) as representing ‘natural’ densities.However, perception is susceptible to thephenomenon of creeping normalcy (Diamond,2005) and it is quite possible, or even likely, thatmuch higher ‘climax’ densities on unexploited reefsediments prevailed in the past. Epibenthic tropicalsea cucumbers, as adults, have few predators(Preston, 1993) thus, on undisturbed reef-associatedhabitats, population densities can build up eitherdue to successive recruitment of sexually derivedjuveniles or, for several species in the tropics, bynatural, transverse asexual fission (Emson andWilkie, 1980), or a combination of both. However,there is some evidence that, for Holothuria atra andStichopus chloronotus at least, population densitiesremain relatively stable following periods of intenseasexual reproduction (Uthicke, 2001c).

Densities below ‘threshold’ levels envisaged byKinch et al. (2008a), or comparable values for otherbêche de mer species, result in increased averageinter-individual distances that, for non-aggregating,broadcast-spawning species, may impair fertilizationsuccess, thus ultimately reducing or delayingrecruitment to the adult populations. Thisinterpretation, in essence operation of the Alleeeffect (Stephens et al., 1999), is supported byevidence that cessation of fishery pressure ondepleted sea cucumber stocks does not result in arapid or marked recovery of stocks (Uthicke et al.,2004; Ahmed and Lawrence, 2007; Kinch et al.,2008a; Price et al., 2013). Large-bodied bêche-de-merspecies may be particularly vulnerable in this regardas their biomass per hectare corresponds to lowerpopulation densities (and thus increased average



inter-individual distances) than for a similar biomassof small-bodied species (Lawrence, 1980). Becausefertilization success is density dependent it is likelythat, at very low densities and without an externalsource of larval/juvenile recruits, economic pressureon the resource can continue beyond the tippingpoint where relaxation of remnant populations andlocal ecological extinction would occur.

Fishery statistics for sea cucumbers are,unfortunately, lacking for the Bunaken area andfor North Sulawesi generally but verbal reports(cited in Lane, 1999b) indicate that intensiveharvesting, before establishment of the BNMP in1991, probably brought stock densities on reefslopes to their present low levels. Size–frequencydata for remnant BNMP populations of the fivemost abundant species (Figure 2) show very lownumbers or absence of small size classes, notablyfor the low-value species, Thelenota anax, perhapssuggesting a failure of recruitment. However,juveniles of tropical, reef-associated sea cucumbersare infrequently observed in the wild andrecruitment ecology is generally poorly understoodfor these invertebrates (Mercier et al., 1999; Shiell,2004; Trentin, 2011).

Reduction of stocks for non-aggregating,broadcast-spawning sea cucumbers to belowthreshold densities may result in drastically reducedsexual reproductive success and consequent failureof natural recruitment and population recovery,even within a protected marine park. Furthermore,it should also be noted that the BNMPmanagement plan of the late 1990s (Mehta, 1999)and subsequent zoning revisions (Erdmann andMerrill, 2004) make no mention of sea cucumberresources or their protection. Thus it is possible thatcontinued low-level exploitation is occurring. TheBNMP area has developed a high internationalprofile in terms of diving and ecotourism, anindustry which has a self-interest in the preservationof marine resources (particularly photogenic species)and which, through the collection of park entrancefees, funds marine policing and conservationmeasures. What is needed in addition, with regard tosea cucumber management, are more extensivesurveys repeated at intervals to monitor populationrecoveries, if any, accompanied by the inclusion inthe park management plan of core zones and

no-take areas for commercial species. Artificialaggregation of pre-spawning adults in protectedareas, to overcome potentially severe spermlimitation effects (Levitan and Petersen, 1995; Yund,2000), could be undertaken as a low-cost research/management initiative that offers the prospect ofrecovery of populations (Bell et al., 2008) and mightlead eventually to a sustainable bêche-de-mer fisherywithin the park.

Overfishing and stock depletion of bêche-de-merat BNMP exemplifies what has been happening inrecent decades to this high-value resource on awider scale globally in the tropical Indo-Pacific(Conand and Byrne, 1993; Anderson et al., 2011;Purcell et al., 2011). Serial population and fisherycollapse throughout the tropical Indo-Pacific,brought about by the overexploitative practices ofbêche-de-mer traders and entrepreneurs have,following the ‘boom times’, incurred consequentiallosses in sustainable revenue for small Indo-Pacificisland nations and their coastal communities - tothe point where a link between overexploitationand low Human Development Indices has beendemonstrated (Purcell et al., 2011).

In addition, there may be significant, but as yetunder-researched, effects on reef ecosystemproductivity, functioning, and resilience resultingfrom the wholesale removal of thesemacrodetritivorous, seabed sediment processors(Wolkenhauer et al., 2010; Anderson et al., 2011;Friedman et al., 2011). Echinoderms, particularlyaspidochirotid sea cucumbers, are a prominent ifnot dominant component of the benthic marinefauna, in both the tropics and at high latitudes, andthey play a key role in structuring many marineecosystems (Uthicke et al., 2009). Aspidochirotidsare in effect earthworms of the sea; their importantcontribution to sediment turnover (Coulon andJangoux, 1993; Uthicke, 1999) and carbon cycling(Moriarty et al., 1985) is well known, yet knowledgeof the ecological impact of wholesale removalthrough overharvesting of these large invertebrates ispoor (Eriksson et al., 2012a). Recent studies indicatethat the sediment-feeding/organic-recycling activitiesof dense populations are important for microalgal(Uthicke, 2001b) and seagrass bed (Wolkenhaueret al., 2010) productivity, nutrient cycling (Uthicke,2001a), and potentially in the CaCO3 balance on



reefs (Schneider et al., 2011). Sand flats and slopesaccount for large areas in and around many coralreefs (Moriarty et al., 1985) and at unexploited, highdensities, populations of aspidochirote seacucumbers, feeding on carbonate sediments, arecalculated to be a greater contributor to night-timedissolution of calcium carbonate and alkalinity thanendolithic carbonate bioeroders (Schneider et al.,2011) thus potentially countering the effects of oceanacidification on reefs, at least locally. Dense seacucumber populations may promote reef health andresilience in another way. Sheltered reef-associatedsediment fields with low sea cucumber abundances inthe west Pacific are often noted to be characterized byundisturbed microalgal mats (observations of the firstauthor). Further investigation and quantification isneeded but it is quite possible that feeding andbioturbation by sea cucumbers may be important incontrolling the build-up of potentially harmfulmicroorganisms and cyanobacterial mats (Bruckneret al., 2003). In essence, these non-charismaticanimals, the literature of which is often relegated toobscurity, may hold one of the keys to the ecologicalintegrity of reefal habitats.

Management of tropical sea cucumber fisherieshas, historically, either been non-existent orinefficient (Choo, 2008; Toral-Granda et al.,2008a) yet even while the bêche-de-mer resourcehas experienced intense fishing pressure andbecome heavily overexploited, the marketdemand for this high-value product continues, tothe ultimate detriment of coastal communitylivelihoods and, potentially, reef resilience. Arecent development and concern is that as thebêche-de-mer resource has become depleted,buyers and harvesters have begun to target notonly lower value species (Kerr, 2013) andsmall-sized individuals (Kinch et al., 2008a, b),but in several Indo-Pacific areas are now shiftingtheir extractive efforts to nocturnal species,particularly infaunal ones that emerge at night(Kinch et al., 2008b; Dissanayake et al., 2010;Choo, 2012; Suharsono pers. comm. – Indonesia).This trend, if permitted or tolerated on a broadgeographic scale, might result in furtheradverse ecological consequences for reef- or seagrass-associated benthic ecosystems, and theirsustainable exploitation.

ACKNOWLEDGEMENTS

The authors express their thanks to the divingsection of Cha Cha Nature Resort on BunakenIsland for their logistical support during the morerecent visits and surveys, and in particular toSoleman Laikun for assistance during the seacucumber transect surveys. Thanks are also due toGustav Paulay and Alexander Kerr for assistancewith identification of some problematic species.Partial funding for the field work was providedinitially from an EEC/National University ofSingapore grant (CL1-CT91-0909), then subsequentlyfrom a Universiti Brunei Darussalam ResearchGrant (UBD/PNC2/2/RG/1(20)).

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